Revista Brasileira de Entomologia 59 (2015) 301–306 REVISTA BRASILEIRA DE Entomologia A Journal on Insect Diversity and Evolution w ww.rbentomologia.com Systematics, Morphology and Biogeography Immature stages of Hamadryas fornax fornax (Hübner) (Lepidoptera: Nymphalidae: Biblidinae) a,∗ b a Lucy Mila Garcia Salik , Luis Anderson Ribeiro Leite , Fernando Maia Silva Dias , a a Mirna Martins Casagrande , Olaf Hermann Hendrik Mielke a Departamento de Zoologia, Universidade Federal do Paraná, Curitiba, PR, Brazil b Laboratório de Entomologia, Departamento de Biologia, Universidade Federal de Sergipe, São Cristóvão, SE, Brazil a b s t r a c t a r t i c l e i n f o Article history: The external morphology and biology of the immature stages of Hamadryas fornax fornax (Hübner, [1823]) Received 12 August 2014 (Lepidoptera, Nymphalidae, Biblidinae) recorded on Dalechampia triphylla (Euphorbiaceae) in Curitiba, Accepted 4 August 2015 Paraná, Brazil are described. Morphological characters are illustrated and described, as a result of obser- Available online 1 October 2015 vations in scanning electron, stereoscope and optical microscopes, the last two attached to a camera Associate Editor: Luis Parra lucida. Results are compared and discussed with immature stages of other species of Biblidinae. © 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open Keywords: Bionomy access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). Life cycle Neotropical Papilionoidea Introduction on the ventral side of the hind wing (Jenkins, 1983). Immatures are associated to plants of the genus Dalechampia (Euphorbiaceae) Hamadryas Hübner, [1806] (Lepidoptera: Nymphalidae: Biblid- (D’Almeida, 1922; Costa Lima, 1936; Armbruster, 1982, 1983; inae) encompasses 20 species and 33 subspecies (Lamas, 2004); Jenkins, 1983; Neild, 1996; Canals, 2003; Pastrana, 2004). Females these butterflies are popularly known as crackers, due to the are similar to males, but frequently with larger size and forewings characteristic noise some species produce while flying (Jenkins, with a more rounded shape (Figs. 1–4) (Jenkins, 1983). 1983; Otero, 1991; Monge-Nájera, 1992, 1995; Monge-Nájera and Despite the large amount of data on the geographic distri- Hernández, 1993; Monge-Nájera et al., 1998; Yack et al., 2000; bution and host plants found in the literature (Jenkins, 1983; Marini-Filho and Benson, 2010; Murillo-Hiller, 2011). They are DeVries, 1987; Neild, 1996; Pastrana, 2004; Contreras Chialchia restricted to the Americas and occur in tropical and subtropi- and Contreras Roqué, 2010), currently there is information on cal forests, savannas, arid and semi-arid lands (Jenkins, 1983). the morphology and biology of immature stages of only eight Hamadryas fornax (Hübner, [1823]) has two recognized subspecies species: H. feronia feronia (Linnaeus, 1758), (D’Almeida, 1922); H. (Lamas, 2004): H. fornax fornax (Hübner, [1823]) with South amphinome amphinome (Linnaeus, 1767) (D’Almeida, 1922; Müller, American distribution from Venezuela to Argentina and H. fornax 1886; Muyshondt and Muyshondt, 1975a); H. fornax fornax (Hüb- fornacalia (Fruhstorfer, 1907) distributed from the South of United ner, [1823]) (Müller, 1886); H. februa februa (Hübner, [1823]) States to the Northern part of Colombia and Venezuela (DeVries, (Comstock and Vasquez Garcia, 1961; D’Almeida, 1922; Muyshondt 1987; Jenkins, 1983; Neild, 1996; Lamas, 2004). and Muyshondt, 1975b; Young, 1974); H. arete (Doubleday, 1847) Hamadryas fornax fornax (Hübner, [1823]) usually perches (Müller, 1886); H. guatemalena guatemalena (H. W. Bates, 1864) upside down on tree trunks on valleys of rivers and clearings in for- (Muyshondt and Muyshondt, 1975c) and H. epinome (C. Felder est habitats and despite its similarity with the other species of the & R. Felder, 1867) (Müller, 1886; D’Almeida, 1922; Leite et al., genus, it is distinguished by its forewing on the ventral surface with 2012b). the proximal area of the discal cell presenting white or grayish- It is widely known that data on the immature stages are impor- white coloration, rarely pale-yellow and the mustard coloration tant for taxonomic and phylogenetic studies of Lepidoptera (Freitas et al., 1997; Freitas and Brown, 2004); therefore this study aims to provide information and extend the knowledge on the subfamily ∗ Corresponding author. E-mail: [email protected] (L.M.G. Salik). http://dx.doi.org/10.1016/j.rbe.2015.08.002 0085-5626/© 2015 Sociedade Brasileira de Entomologia. Published by Elsevier Editora Ltda. This is an open access article under the CC BY-NC-ND license (http://creativecommons.org/licenses/by-nc-nd/4.0/). 302 L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306 Figs. 1–4. Hamadryas fornax fornax (Hübner, [1823]). 1, 2. Male: 1, dorsal view; 2, ventral view; 3, 4. Female: 3, dorsal view; 4, ventral view. Scale bar: 1 cm. Biblidinae by describing the external morphology and the biology same color of the pronotal plate. Body translucent yellowish ochre, of the immature stages of H. fornax fornax. with rounded white spots regularly distributed on the dorsal and lateral areas. Numerous spiniform or clavate black setae distributed along the body, most of them on chalazae. Bases of all black setae Material and methods forming circular blackened areas interspersed with white rounded ◦ areas. Spiracles of T1 and A8 elliptical and similar; other spiracles Eggs were collected in the Parque Municipal Barigui (25 25 S, ◦ smaller and rounded. After the eclosion, the larvae are not gregar- 49 18 W, 910 m), Curitiba, Paraná, Brazil, along with branches ious, and feed independently. Chaetotaxy is given by Figs. 19–21. of the host plant Dalechampia triphylla Lam. (Euphorbiaceae) Head capsule: width: 0.65 mm; height: 0.68 mm. Average length and reared in laboratory (Laboratório de Estudos de Lepidoptera of the larva before molting: 5 mm. Average duration: 3 days (n = 9). Neotropical at the Universidade Federal do Paraná). Laboratory pro- cedures, such as the maintenance of the samples and the host plant, preparation and observation of the structures using stereoscopic Second instar (Figs. 11, 23) microscope, drawings, photographs, scanning electron microscopy Head capsule black. Epicranium with a pair of short truncated and terminology follows Leite et al. (2012b) and other recent stud- dorsal scoli. Setae on lateral and lateroventral regions of the epi- ies on immatures of Biblidinae (Leite et al., 2012a, 2014). Voucher cranium on cream-colored chalazae. Prothorax yellow ochre, with specimens are deposited at the Colec¸ ão Entomológica Pe. Jesus black and distally creamy white scoli. Remaining segments olive Santiago Moure; Universidade Federal do Paraná, Curitiba, Paraná, brown with a narrow yellow ochre lateral band in A1–A10, at the Brazil. level of the supraventral setae. Thorax and abdomen with subdor- sal black and distally creamy white scoli on T2, T3, A7 and A8, Results remaining scoli translucent yellow. Head capsule: width: 1.04 mm, height: 0.95 mm. Length of the Hamadryas fornax fornax (Hübner, [1823]) (Figs. 1–29) dorsal protuberance: 0.44 mm. Average length of the larva before molting: 6 mm. Average duration: 3 days (n = 8). Egg (Figs. 5–9) Elliptical, with several irregular carinae and flattened on the bot- Third instar (Figs. 12, 24) tom pole. Uniformly pearly white in color. Micropilar region on the Head capsule black; dorsal scoli longer than the previous instar, upper pole in the center of a round and slightly concave area. blackened and with spiniform setae. Thorax and abdomen with the Oviposition is normally gregarious; the eggs are laid on the same coloration of the head, except for the yellow ochre supraven- upper side of the host plant Dalechampia triphylla, one on top of tral and ventral areas. Most of the thoracic and abdominal scoli each other, the first instar hatch laterally. black, except for some lateral translucent yellow scoli from A3 to Diameter: 1.01 mm. Average duration: 8 days (n = 15). A6. Head capsule: width: 1.63 mm; height: 1.66 mm. Length of the First instar (Figs. 10, 19–22) dorsal protuberance: 2.7 mm. Average length of the larva before Head rounded, black, and without scoli. Frons ventrally delim- molting: 13.5 mm. Average duration: 4 days (n = 7). ited by the clypeus, which appears as a sclerotized transverse band. Labrum bilobed. Mandibles strongly sclerotized with a serrated cut- ting edge. Six stemmata latero-ventrally, 1–4 and 6 arranged in Fourth instar (Figs. 13, 25) semi-circle and 5 ventrally, and closer to the base of the antenna. Head capsule similar to the previous instar. Prothorax anteri- Pronotal plate black and divided, forming two sub-rectangular orly reddish-brown, with black pronotal plate. Dorsally, two pairs plates, with four pairs of setae on chalazae. Thoracic legs with the of yellow longitudinal bands from T2 to A9. Reddish-brown band L.M.G. Salik et al. / Revista Brasileira de Entomologia 59 (2015) 301–306 303 Figs. 5–18. Hamadryas fornax fornax (Hübner, [1823]). 5–9. Egg: 5, SEM lateral view; 6, SEM lateral view of the egg-laying; 7, lateral view; 8, dorsal view; 9, lateral view of the egg-laying. 10–15. Larvae: 10, 1st instar; 11, 2nd instar; 12, 3rd instar; 13, 4th instar; 14, 5th instar lateral view; 15, 5th instar dorsal view. 16–18. Pupae: 16, ventral view; 17, dorsal view; 18, lateral view. SEM – Scanning Electronic Microscopy. Scale bars Figs. 7–8: 0.5 mm, Fig. 9: 1 mm. laterally disposed on T2 and T3 and on the abdominal segments at tudinal bands and an orange lateral band from the spiracular to the the level of the supraventral setae. ventral area. Abdominal legs orange. Head capsule: width: 1.8 mm, height: 1.7 mm. Length of the Head capsule: width: 3.4 mm, height: 3.2 mm. Length of the dorsal protuberance: 3.2 mm. Average length of the larva before dorsal protuberance: 6.38 mm.